Assessing the Current Status of the Yosemite Toad (Anaxyrus [Bufo] Canorus) in the Sierra Nevada, California, Usa

Home , Yosemite toad

Herpetological Conservation and Biology 7(2): 115–131. Submitted: 15 March 2012; Accepted: 17 July 2012; Publication: 10 September 2012.

ADVANTAGES OF LONG-TERM, MULTI-SCALE MONITORING: ASSESSING THE CURRENT STATUS OF THE YOSEMITE TOAD (ANAXYRUS [BUFO] CANORUS) IN THE SIERRA NEVADA, CALIFORNIA, USA

1 CATHY BROWN , KATIE KIEHL, AND LUCAS WILKINSON

USDA Forest Service, Stanislaus National Forest, 19777 Greenley Road, Sonora, California 95370, USA 1Corresponding author, email: [email protected]

Abstract.—A comprehensive bioregional evaluation of the current status of at-risk species is critical for effective management and conservation. As part of a long-term, multi-scale amphibian monitoring program, we evaluated the current status of the Yosemite Toad (Anaxyrus [Bufo] canorus) on national forest lands across the species’ range in the Sierra Nevada, California, USA. We conducted monitoring at extensive (rangewide) and intensive (individual population) scales with small watersheds (2–4 km2), individual meadows, and breeding areas within meadows as sample units. Yosemite Toad breeding was found in an estimated proportion of 0.84 ± 0.03 (SE) of recently occupied watersheds (locality data from 1990–2001), and 0.13 ± 0.04 of historically occupied watersheds (locality data prior to 1990). Rangewide, breeding was found in an estimated proportion of 0.22 ± 0.01 of watersheds. We quantified demographic parameters (abundance and survival of breeding males, abundance of egg masses, successful metamorphosis) in six meadows in two watersheds. Abundances were small, with the largest populations having only 16–21 and 18–19 breeding males each year. Annual survival rates of males by meadow ranged from 0.49–0.72. Numbers of egg masses per year were low, and the proportion of breeding areas with successful metamorphosis ranged from 0.14–0.73. Using the multi- scale data, we examined Yosemite Toad spatial and temporal occupancy patterns. Yosemite Toads tended to breed in one or two sites (lakes, meadows, stream reaches) per watershed every year, and occasionally in other sites. This assessment of the status of the Yosemite Toad will inform management decisions at both bioregional and population scales and the development of conservation priorities.

Key Words.—amphibian demography; Anaxyrus canorus; bioregional monitoring; multi-scale monitoring; Sierra Nevada; Yosemite Toad

INTRODUCTION al. 1991; Hecnar and M'Closkey 1997; Meyer et al. 1998; Skelly et al. 2003; Trenham et al. 2003). Amphibians are imperiled worldwide (Beebee and Logistically, the types of data that are feasible to collect Griffiths 2005; Wake and Vredenburg 2008) and over at bioregional and local scales differ (see Beebee and 40% of all amphibian species have decreasing Griffiths 2005). Detailed abundance and demographic population sizes (Stuart et al. 2004). As efforts to data provide the most insight into population dynamics, identify and monitor at-risk populations have increased, but are usually too expensive and logistically impractical the role of spatial and temporal scale in providing robust to collect long-term and over large geographic areas. As assessments of status and understanding the population a result, researchers increasingly use occupancy data as a dynamics of amphibians has come to the forefront more cost-effective alternative (Trenham et al. 2003; (Hecnar and M'Closkey 1997; Meyer et al. 1998; Skelly Bailey et al. 2004; Corn et al. 2005; Gould et al. 2012). et al. 2003). Many population studies have been However, occupancy data alone provide no information conducted at local scales such as individual lakes or on changes in abundance, which may be a first sign of ponds and often over short time periods (Briggs and impending distributional declines (Muths et al. 2003; Storm 1970; Pechmann et al. 1991; Richter and Siegel Weir et al. 2009; Collen et al. 2011), or key vital rates 2002). However, bioregional assessments, generally and life-stage specific population dynamics (Berven conducted over large areas often defined by ecological 1990; Semlitsch et al. 1996; Biek et al. 2002; Scherer et characteristics, are needed to fully evaluate a species al. 2005). One solution is to collect occurrence data status (Stuart et al. 2004; Gompper and Hackett 2005; across bioregional scales to evaluate rangewide Bonardi et al. 2011; Cameron et al. 2011; Gould et al. persistence and more detailed demographic data at a 2012), and monitoring over broader spatial and temporal smaller subset of locations to provide insights on local scales may be more effective at separating general population dynamics such as abundance, survival, and population trends from local fluctuations (Pechmann et recruitment (e.g., Corn et al. 1997).

Brown et al.—Current Status of the Yosemite Toad.

The Yosemite Toad (Anaxyrus [Bufo] canorus) is a lentic water) within sites. In this paper, we present a species well suited for a multi-scaled monitoring baseline assessment of bioregional population status for approach. The Yosemite Toad is endemic to the Sierra the Yosemite Toad. We also show how data collected Nevada, California, where it occurs predominantly on for status and trend can be used to address other public lands (almost 99% of its range), much of which is questions useful for management by presenting insights in wilderness areas. Declines in the Yosemite Toad have on Yosemite Toad spatial and temporal occupancy been documented (Kagarise Sherman and Morton 1993; patterns. Jennings and Hayes 1994; Drost and Fellers 1996), and the U.S. Fish and Wildlife Service has determined that MATERIALS AND METHODS listing the species as endangered under the Endangered Species Act is warranted but precluded by higher Study region.—The study region for the extensive priority actions (U.S. Fish and Wildlife Service 2002). component is the portion of the historical range of the However, a comprehensive assessment of status across Yosemite Toad that occurs on national forest lands the species' range has not previously occurred and within the Sierra Nevada, California, USA (Fig. 1). This potential causes of decline are not well understood. area comprises about 10,500 km2 extending from Alpine There are multiple challenges to monitoring the County south to Fresno County and contains survey Yosemite Toad. If surveys are timed correctly, all life watersheds at elevations from 1,859 to 3,703 m. Aquatic stages are relatively easy to detect; however, the suitable habitats within the study region are chiefly fed by survey periods for each life stage are relatively short and snowmelt, and include lakes, ponds, wet meadows, and are not concurrent. Breeding commonly occurs in streams, which vary greatly in size, vegetation, shallow, warm water areas that typically dry over the hydrology, and topography. A variety of management summer and include wet meadows, shallow ponds, activities occur within the study region although much is shallow flooded, grassy areas adjacent to lakes, and slow in designated wilderness where management activities flowing streams (Karlstrom 1962). Yosemite Toads are are more limited and access is only by foot or pack explosive breeders where adults arrive at snowmelt, lay animal. Livestock grazing occurs in many Sierran eggs over a short period of time, and then leave the meadows and legacy effects exist even in those areas breeding areas (Kagarise Sherman 1980). Because they where grazing no longer occurs (Menke et al. 1996). are not commonly found after breeding, surveys for Fish stocking has occurred since the late 1800's and is adults must occur at snowmelt over a 1–2 week period, still widespread (Bahls 1992; Knapp 1996), and when most locations are difficult to access. Eggs hatch recreational activities are increasing in high elevation into larvae in about 4–15 days (Karlstrom 1962; wilderness areas (USDA Forest Service 2001). Other Kagarise Sherman 1980), tadpoles often metamorphose activities such as vegetation, fire and fuels, and road by early to mid August (Karlstrom 1962; pers. obs.), and management also may affect the species at lower metamorphs disperse from immediate breeding areas elevations. (pers. obs.). The rapid development, desiccation of The two intensive watersheds included Bull Creek ephemeral breeding areas, and dispersal behavior result (4.86 km2), located in Fresno County in the southern in a short survey window for each of these stages, which, Sierra Nevada, and Highland Lakes (2.9 km2), located in combined with the remote locations of much of the Alpine County in the central Sierra Nevada (Fig. 1). species’ range, makes it logistically difficult to collect Elevations in Bull Creek range from 2,134 m to 2,489 m demographic information on all life stages over and vegetation is predominantly forested with small bioregional scales. meadow and riparian openings (0.33 ha to 5.1 ha). To provide a comprehensive bioregional assessment of Management activities occurring in the watershed the status of the Yosemite Toad that addressed these include livestock grazing, recreation, timber harvest, and monitoring challenges, the USDA Forest Service ongoing ecological research. Highland Lakes, situated implemented a long-term multi-scale monitoring in a saddle surrounded by high peaks, is chiefly open program on national forest lands in the Sierra Nevada. with large areas of alpine meadow containing numerous In an extensive component, we estimated the proportion small pools and areas of flooded vegetation. Elevations of occupied watersheds at the scale of the range of the of suitable Yosemite Toad habitat range between 2,536 Yosemite Toad on national forest lands using a spatially m and 2,621 m. This watershed contains a popular balanced, unequal probability survey design. In an campground and draws large numbers of visitors for intensive component, we estimated abundance and both summer and winter recreational activities. survival of adult breeding males, number of egg masses, Livestock grazing also occurs in the watershed. and successful metamorphosis in six meadows in two watersheds. Between the two components, we Design and field methods extensive component.— conducted surveys at three scales, watershed, site (lake, Probability-based survey designs such as the one used in meadow, stream reach), and breeding area (contiguous this program require a precisely defined target

116

Herpetological Conservation and Biology

FIGURE 1. Study region and distribution of known occupied watersheds for the Yosemite Toad (Anaryxus canorus) in the Sierra Nevada, California, USA. The monitoring area is national forest lands within the range of the Yosemite Toad. Bull Creek and Highland Lakes are the two Yosemite Toad intensive watersheds

population (i.e., the set of units defining the geographic not feasible to create one (i.e., delineate all 2–4 km2 scope of inference) and a sample frame (commonly a watersheds within the monitoring area), we used the geographic information system [GIS] representation of Forest Inventory and Assessment (FIA) systematic the target population) from which the sample is selected random hexagonal grid (Brand et al. 2000) densified to (Olsen et al. 1999). We defined our target population as hexagons of 2.6 km2. all watersheds, delineated to 2–4 km2 in size, with We compiled all available Yosemite Toad locality data available aquatic habitat on national forest lands within from state and federal agency records, academic the range of the Yosemite Toad. Because there was no researchers, and from literature and museum sources. existing sample frame (e.g., GIS coverage) and it was We assigned each of the 10,077 hexagons (and

117

Brown et al.—Current Status of the Yosemite Toad. corresponding grid point centers) in the sample frame to Design and field methods intensive component.—We one of three mutually exclusive temporal categories subjectively selected two intensive watersheds using the based on the compiled locality data: (1) Recent, toads following criteria: (1) contained a variety of aquatic documented within 10 years prior to the start of the habitat types; (2) contained at least three breeding lakes, sampling (defined to be after 1990); (2) Historical, toads meadows, or stream reaches separated by more than 200 documented only prior to 1990; and (3) Unknown, no m; (3) supported a relatively large number of adult toads; locality data. A spatially distributed random sample was and (4) had easy access at snowmelt and during the selected from the sample frame using a generalized summer. From 2006–2009, we visited three meadows in random tessellation stratified survey design (GRTS) for each watershed at snowmelt to conduct adult capture- a finite resource with unequal probability of selection mark-recapture (CMR) and egg mass surveys (Bull based on the three temporal categories (Stevens and Creek meadows: 520M15, 520M16, 520M20; Highland Olsen 1999; Stevens and Olsen 2004). We selected a Lakes meadows: 37188, 37213, 37165). The ecology of larger proportion of the sampled hexagons from areas the Yosemite Toad is ideal for using Pollock's robust most likely to have Yosemite Toads (Recent). We design (Pollock 1982; Kendall et al. 1997) to estimate delineated watersheds, 2–4 km2, around the selected grid abundances of breeding males during their spring point centers using the Hydrologic Unit Code rule set chorus. The robust design is two-tiered with primary (U.S. Department of Agriculture 1997). sampling periods that occur over longer intervals that Temporally, the study design uses an augmented allow population gains (recruitment/immigration) and serially alternating panel design (Urquhart et al. 1998; losses (mortality/emigration), and secondary sampling Urquhart and Kincaid 1999). The initial design specified occasions within each primary period where the that 20% of the Recent watersheds (n = 16) were to be population is assumed to be closed. We treated each visited every year (referred to as the annual watersheds), annual breeding period as a primary sampling period. and the remaining watersheds once every five years on a Because males congregate in breeding choruses for the rotating schedule. Due to funding limitations, the full short duration of the breeding period, we treated multiple sample of watersheds took eight years to complete samples over consecutive days during each primary (2002–2009). Based on preliminary analyses of the first period as secondary occasions from a population that is five years of data, we determined that completing the relatively closed. The robust design is not as suitable for full sample, thereby increasing the precision of the estimating female abundances. Female toads remain in estimates, was more important than beginning the breeding areas for only a few days leaving shortly after second cycle. amplexus, thus violating the assumption of population We determined watershed occupancy by surveys of all closure among the secondary occasions. Still, we lentic (lakes, wet meadows) and a sample of lotic habitat marked females when possible. (perennial and ephemeral streams) within each We conducted CMR surveys as soon as breeding watershed. We identified lakes and meadows using choruses formed at snowmelt and surveys continued for aerial photographs that we verified in the field. We at least five consecutive days each year. The timing of randomly selected three 300-m perennial stream reaches snowmelt and the subsequent breeding varied among per watershed, one from each of three gradient classes years ranging from late April to mid May in Bull Creek (low < 2%, medium 2–8%, and high > 8%), and two and from late May to late June at Highland Lakes. We 100-m ephemeral stream reaches located in meadows surveyed each intensive meadow for at least six hours from a USDA Forest Service Sierra-wide GIS coverage each day. At each meadow, crews rotated among the (Region 5 Remote Sensing Lab in 2001, available from breeding choruses, visually scanning the breeding areas, Cathy Brown). We refer to the individual lakes, actively searching in burrows and under ground cover, meadows, and selected stream reaches in each extensive and using cues from calling males to locate toads. All watershed as sites. unmarked toads > 40 mm snout-urostyle length (SUL) From June-September 2002–2009, we used Visual were PIT-tagged (passive integrated transponder; Martin Encounter Surveys (VES) to determine Yosemite Toad 2008) using AVID MUSICC MicrochipsTM (Avid occupancy in each extensive watershed (Crump and Identification Systems, Inc., Norco, California, USA) Scott 1994; Olson et al. 1997). We surveyed all and released. Upon initial capture each year, we wadeable water at each site (lake, meadow, and selected recorded the snout-urostyle length, weight, and sex of stream reach) and we made an effort to survey each toad. We identified marked animals by their watersheds early in the season before sites dried up to unique tag numbers at each subsequent recapture, and maximize detection of the tadpole stage. Although our we used these data to create capture histories. primary goal was to detect tadpoles, we recorded data on We conducted egg mass counts at the end of the five all life stages observed. day adult CMR period. Conducting counts of Yosemite Toad egg masses can be challenging because females lay eggs in long strings and sometimes split masses over two

118

Herpetological Conservation and Biology or more locations or lay them communally. Also, eggs moving through an area. Therefore, our primary goal may hatch prior to the completion of the five day period was to estimate the proportion of watersheds occupied or be deposited after counts are conducted. To address () by breeding (eggs, tadpoles, or metamorphs). Too these challenges, we used several methods to determine few adults were found to model them separately, so to the most efficient approach. We used the more intensive account for all areas occupied by the species, we also dependent double-observer method (Grant et al. 2005) in estimated the proportion of watersheds occupied by any 2006 and independent double-observer method (Nichols life stage. For both occupancy states (breeding, any life et al. 2000) in 2007 and 2008. After employing and stage), we estimated the proportion of occupied testing these multiple observer methods, individual egg watersheds for the entire range of the species mass detection probabilities were very high (> 0.96) and (rangewide, (.) ) and relative to the temporal period consistent among observers. Accordingly, in 2009 we when toads were last observed (Recent, Historical, simply used a tally of unique eggs masses (i.e., Unknown, (temporal category) ). We used a maximum conditional probability of detection = 1) from a single likelihood approach that incorporates the probability of observer. This was simpler and more efficient, and in detecting the species (p) and the watershed weights our judgment, an accurate estimate of the number of (described below; also MacKenzie et al. 2006). Methods Yosemite Toad masses laid each year. Although the that do not account for p typically result in an methods differed among years, the estimates of egg mass underestimate of occupancy unless the probability of numbers were similar and reasonable given the numbers detection is near one (MacKenzie et al. 2006). We of adults we observed. Thus, in our judgment, the three assumed that the occurrence of toads was closed during methods were comparable. In addition, based on our the eight-year monitoring period (i.e., occupancy state in observations during the five day period and our each watershed did not change) and used the annual subsequent surveys of these meadows for the extensive watershed data to estimate the probability of detection. component, it is unlikely that we missed large numbers This approach differs from most studies where visits of egg masses. occur over shorter time periods, typically within a In 2006, we visited each intensive meadow every two season. If the population closure assumption is violated, weeks (Bull Creek 29 June - 25 August; Highland Lakes the probability of occupancy may be overestimated. We 12 July - 7 September) for a total of six visits. At each recognize that eight years may be a long time to assume breeding area in each intensive meadow, two observers that watershed occupancy is constant. Our approach independently counted tadpoles and metamorphs. may be reasonable given the likely slow and persistent Additional surveys were conducted by one observer at effects resulting from many management activities, but Bull Creek once per week (10 visits, 17 June - 19 be more questionable for threats such as an epidemic August) in 2009 and at Highland Lakes once every two pathogen that causes widespread and rapid declines. We weeks (five visits, 15 June - 27 August) in 2007 and address this assumption and its implications in our twice (14 July, 29 July) in 2008. These data were used discussion. to document successful metamorphosis for each We modeled p as a function of two covariates, survey breeding area. date (measured by the number of days from January 1) and snow pack of the preceding winter. Snowpack was Analysis extensive component.—We based the quantified as the percentage of normal snowpack for the analyses of occurrence data on an unequal probability Sierra Nevada measured on 1 April each year (California survey design where the weight for each watershed Department of Water Resources, California Data evaluated is the inverse of the probability of selection for Exchange Center. Available from http://cdec.water.ca. that watershed (Diaz-Ramos et al. 1996). The gov/ [Accessed 17 September 2009]). The Sierra contribution of each sample watershed to the final Nevada receives most of its precipitation between estimate is proportional to the watershed weight. For December and April (Howat and Tulaczyk 2005). Date example, sample watersheds with higher probability of of survey and seasonal water are important factors for selection (e.g., Recent watersheds) have lower weights detecting many amphibian species (Schmidt 2005; Weir and thus contribute less to the final estimate. We et al. 2005; Lacan et al. 2008). Yosemite Toads breed in conducted analyses using the R software (R ephemeral habitats and metamorphose within one Development Core Team, Vienna, Austria), an R summer. Thus, we predicted that p should be highest in contributed library (spsurvey: Spatial Survey Design and early season surveys and in years with higher snow pack Analysis, Kincaid and Olsen 2009) developed for the (i.e., more available water). Habitats dry up sooner in statistical analysis of probability survey data, and SAS® drought years, so we tested for a survey date and snow software (SAS Institute Inc., Cary, North Carolina, pack interaction. We developed ten a priori models USA). where ψ = probability of occupancy and p = probability The presence of tadpoles indicates the existence of a of detection (Table 1). reproducing population rather than, for example, an adult We used a generalized version of the maximum

119

Brown et al.—Current Status of the Yosemite Toad.

TABLE 1. Model selection for occupancy estimates for the Yosemite Toad (Anaryxus canorus) for breeding and any stage, summarized rangewide and by temporal category. K is the number of parameters in the model. AICc is the Akaike Information Criterion adjusted for small sample sizes. wi is the Akaike weight for comparing models. ψ is the probability of occupancy and p is the probability of detection. Models comprising ≥ 95% of the weight are in bold.

Breeding Any Stage

Model K AICc ΔAICc wi Model K AICc ΔAICc wi Rangewide, ψ (.) p(Survey Date * Snow Pack) 5 1851.7 0.0 0.996 p(Survey Date * Snow Pack) 5 2059.9 0.0 1.000 p(Snow Pack) 3 1862.8 11.1 0.004 p(Survey Date + Snow Pack) 4 2232.0 172.2 0.000 p(Survey Date + Snow Pack) 4 1885.2 33.5 0.000 p(Snow Pack) 3 2276.0 216.2 0.000 p(.) 2 2027.4 175.7 0.000 p(Survey Date) 3 2368.6 308.8 0.000 p(Survey Date) 3 2029.3 177.6 0.000 p(.) 2 2372.0 312.2 0.000 Temporal Category, ψ (Temporal Category) p(Survey Date * Snow Pack) 7 1459.8 0.0 1.000 p(Survey Date + Snow Pack) 6 1872.7 0.0 1.000 p(Snow Pack) 5 1487.8 28.0 0.000 p(Snow Pack) 5 1909.8 37.2 0.000 p(Survey Date + Snow Pack) 6 1523.4 63.6 0.000 p(Survey Date * Snow Pack) 7 1913.8 41.2 0.000 p(.) 4 1534.1 74.3 0.000 p(.) 4 1955.4 82.7 0.000 p(Survey Date) 5 1538.6 78.8 0.000 p(Survey Date) 5 1957.6 85.0 0.000 likelihood procedure developed by MacKenzie et al. (2002) appropriate for our more complex unequal 1 probability survey design. The following notation is used: S, the number of space-time subunits in the study; where S subunits are present and each watershed has a n the number of watersheds in the sample in subunit s; s, weight, w and V, number of distinct seasonal sampling occasions;  , si, si 0 if ′ 0 probability that a species is present in watershed i within ′ 1 if 0 subunit s; psiv, probability of detecting a species in watershed i within subunit s on visit v, given the species and both si and psiv may depend on the covariates. The term distinguishes the watersheds where a is present. Then let ,,…, where species is detected on at least one visit and those sites 1 if species is detected in watershed i in where a species is not detected on any visits. This is the subunit s on visit v same likelihood equation as in MacKenzie et al. (2002) when all weights are equal, as is the case for a simple d = 0 if species is not detected in watershed siv i in subunit s on visit v random sample. We maximize the log likelihood using NA if no visit was made in watershed i in the function “optim” in R (R Development Core Team, subunit s on visit v Vienna, Austria). Variance estimates for and are obtained from the Fisher information matrix derived and s=1,…,S, i=1,…,ns and v=1,…,V. Let from the Hessian matrix evaluated at the and ,,…, be K watershed-specific covariates estimates. Confidence intervals are constructed as the for watershed i within subunit s and estimate ± the square root of these variance estimates multiplied by the 1⁄ 2 th percentile of the standard normal distribution. We evaluated the relative support for each model using Akaike Information Criterion for small sample sizes (AICc) and Akaike weights (wi) (Burnham and Anderson 2002). We dropped models be M watershed-specific and visit-specific covariates for that could not be fit to the data from the model set and watershed i within subunit s. The likelihood equation we used the remaining models to compute model- for a stratified unequal probability survey design, such as averaged estimates (Burnham and Anderson 2002; the one used in this program, is MacKenzie et al. 2006).

Analysis intensive component.—We analyzed capture , |, , |, history data for male Yosemite Toads to estimate abundances during spring breeding and apparent annual

survival rates. We designated survival "apparent"

120

Herpetological Conservation and Biology because we cannot distinguish between male Yosemite TABLE 2. Final models and Akaike weights used to estimate numbers Toads that die from those that permanently emigrate of Yosemite Toad (Anaryxus canorus) adult males using the robust design from 2006–2009 in six meadows in two watersheds in the (Williams et al. 2002). We ran analyses separately for Sierra Nevada, California. Models that could not be fit to the data are each of the six intensive meadows (three in each not included. QAICc is the Akaike Information Criterion adjusted for watershed). Because the robust design assumes that small sample sizes and overdispersion. wi is the Akaike weight for populations are closed over secondary occasions (there is comparing models. φ is annual survival rate, p is probability of capture, and c is probability of recapture. no immigration or emigration), we tested for demographic closure for each intensive meadow each Model # Param. QAICc wi year. Examination of the capture histories suggested that Bull Creek Watershed any violation of the closure assumption likely resulted 520M16 from immigration into the meadows during the primary period (i.e., males were not all present at the start of the φ(.)p(.)c(.) 3 269.0 0.538 secondary occasions but once present they tended to φ(.)p(year)c(year) 9 269.9 0.343 remain). Because sample sizes were small, to obtain φ(year)p(.)c(.) 5 273.2 0.066 better fitting models, we chose to test for immigration, φ(year)p(year)c(year) 11 273.7 0.053 but not emigration. This was done by fitting a Pradel 520M15 model (Pradel 1996) with no immigration (recruitment = 0, closed model) and a model allowing immigration φ(.)p(year) 5 178.0 0.486 (recruitment unconstrained, open model, Boulanger et al. φ(.)p(.) 2 179.0 0.286 2002). We compared the closed and open models for φ(year)p(year) 7 180.1 0.164 each meadow and year using likelihood ratio tests. For φ(year)p(.) 4 182.0 0.064 meadows where the closure test suggested that 520M20 populations were not closed, we pooled captures from all but the last visit within each primary period such that φ(year)p(.) 3 67.9 0.873 each primary period included two secondary occasions φ(.)p(year) 4 73.0 0.068 (Kendall 1999). For meadows where populations were φ(year)p(year) 5 73.3 0.059 closed, to reduce the number of models for comparison, Highland Lakes Watershed we conducted exploratory analysis for each meadow 37188 each year by fitting the data to four Huggins closed φ(.)p(.) 2 125.5 0.516 population models where the probability of capture was φ(.)p(year) 5 126.2 0.377 held constant (Mo) or allowed to vary by behavior (Mb), time (Mt), or both (Mtb) (White et al. 1982). For each φ(year)p(.) 4 129.7 0.065 meadow, we chose the closed population model that had φ(year)p(year) 7 130.5 0.043 the most support, based on Akaike weights (wi) using 37213 QAIC values, for inclusion in the robust design analysis. c φ(.)p(.) 2 65.0 0.670 We fit the resulting data to four Pollock’s robust design models where apparent survival (Φ) was held φ(year)p(.) 3 67.2 0.220 constant or allowed to vary among years, and the φ(.)p(year) 4 69.1 0.085 probability of capture (p) and recapture (c) were φ(year)p(year) 5 71.5 0.025 modeled with the best supported closed population 37165 model, and held constant (p(.)), or allowed to vary φ(.)p(.)c(.) 3 116.5 0.668 among years, (p(t)) (Table 2). We did not include temporary emigration because in our preliminary φ(year)p(.)c(.) 4 118.1 0.305 analysis, most models could not be fit to the data or had φ(.)p(year)c(year) 7 123.5 0.020 little support, likely due to small sample sizes and the φ(year)p(year)c(year) 8 125.7 0.007 short study duration (four years). Instead, we compiled the breeding schedules of adult males from the CMR 2002). We used the R (R Development Core Team, data. We used the program RDSurviv (Kendall and Vienna, Austria) package, RMARK (Laake, J., Version Hines 1999) to test the goodness of fit for the most 1.9.6) for model fitting and averaging. general model for each meadow and calculate the 2 For years where we estimated egg mass abundances, variance inflation factor, ĉ , based on the Pearson's X via either the double observer or independent double 2 test (ĉ = X /df, Amstrup et al. 2005). We based model observer methods, we analyzed the data using the selection on Akaike weights (wi) calculated from QAICc program DOBSERV (Hines, J.E., U.S. Geological values (Burnham and Anderson 2002). We calculated Survey, Laurel, Maryland, USA). Two models were fit to abundance and apparent survival estimates by model the data, p(.) and p(observer), where the probability of averaging of the final model set (Burnham and Anderson detection was held constant and allowed to vary among

121

Brown et al.—Current Status of the Yosemite Toad. observers, respectively. Finally, for each year and TABLE 3. Sample sizes for monitoring surveys and the estimated watershed, we calculated the proportion of breeding proportion of occupied watersheds ( ) for the Yosemite Toad (Anaryxus canorus) from 2002–2009. and the standard error (SE) areas where metamorphs were detected. are shown for breeding and any stage rangewide and by temporal category. The estimated # of watersheds is the estimated number of Analysis of spatial and temporal occupancy watersheds of the target size (2–4 km2) within the range of the species. patterns.—We examined temporal and spatial breeding occupancy patterns at three scales: watershed (extensive Range Recent HistoricalUnknown component), site (individual lake, meadow, or stream # Watersheds Surveyed 134 69 20 45 reach in the extensive watersheds), and breeding area # Annual Survey Watersheds 18 12 0 6 (contiguous areas of standing water) in the intensive # Sites Surveyed 2213 1243 273 697 meadows. In this analysis, we included only the annual watersheds where breeding occupancy was detected in at Estimated # Watersheds 3069 213 103 2753 least one survey (n = 14 watersheds) and the intensive Estimated # Watersheds SE 1415 38 64 1415 meadows. Because of the small sample size, our # Breeding 65 45 9 11 objective of examining temporal and spatial patterns  Breeding 0.22 0.84 0.13 0.05 together, and the fact that we did not have multiple surveys within a year to estimate probability of SE Breeding 0.012 0.032 0.038 0.004 detection, we chose a descriptive approach rather than # Any Stage 72 48 10 14 more complex dynamic occupancy modeling (e.g.,  Any Stage 0.29 0.85 0.15 0.08 MacKenzie et al. 2003). This descriptive approach does SE Any Stage 0.013 0.031 0.042 0.005 not incorporate probability of detection. To examine temporal variability, we assigned watersheds, sites, and breeding areas to one of three categories: (1) occupied was found in a relatively large proportion of the Recent every year surveyed; (2) unoccupied only one year; and watersheds ( = 0.84 ± 0.032) compared to only 0.13 ± (3) unoccupied 2+ years. We also examined both 0.038 of Historical watersheds (those occupied prior to temporal and spatial occupancy in combination by 1990). Finally, breeding was observed in an estimated looking at the number of sites per extensive watershed 0.05 ± 0.004 of Unknown watersheds. Occupancy and breeding areas per intensive meadow that were estimates for any stage were similar to those for consistently occupied by breeding. We defined breeding; adults were found in few additional watersheds consistently occupied to be occupied every year or that did not have breeding. unoccupied only one year. We assigned watersheds and intensive meadows to three categories: (1) three or more Intensive component.—The Pradel models could not sites/breeding areas consistently occupied every year; (2) be fit to the mark-recapture data for four meadow-year only one or two sites/breeding areas consistently combinations, probably due to low sample sizes. Based occupied every year; and (3) no sites/breeding areas on the likelihood ratio test, populations were closed in consistently occupied every year. two intensive meadows and open in three intensive meadows most years surveyed; the sixth meadow could RESULTS not be modeled. For the meadow-years with open populations, the parameter estimates for immigration Extensive component.—Within the range of the rates were low (range = 0.06–0.26) suggesting that Yosemite Toad, we surveyed 134 watersheds between violation of the closure assumption was not severe. The 2002 and 2009, including 18 that were surveyed behavior model, Mb (the probability of capture, p, differs annually (Table 3). The interaction model, p(survey date from the probability of recapture, c), had the most * snow pack), had the most weight for both breeding and support in the two intensive meadows where populations any stage occupancy rangewide and for breeding were closed (Table 2). Overall, the goodness-of-fit occupancy by temporal category (Table 1). The best analysis suggested that the most general model model for any stage by temporal category was p(survey adequately fit the data with ĉ values ranging from 1.0– date + snow pack). In general, these models indicated a 1.8. Because there was some overdispersion, we used high probability of detection (≥ 0.8) if surveys are QAICc for our model selection criteria and adjusted the conducted early enough in the season (e.g., prior to mid standard errors by ĉ for each meadow. August) in all but the lowest snow pack years such as The total number of unique individuals captured per occurred in 2007 (snowpack was 45% of average on intensive meadow during the four-year monitoring April 1). period ranged from 4–37 for males and 5–38 for The rangewide occupancy estimate ( ) for the females. Accordingly, annual population estimates were Yosemite Toad was 0.22 ± 0.012 (SE) for breeding and also small (Table ̂ 4). The largest populations in each 0.29 ± 0.013 for any stage (Table 3, Fig. 1). Breeding watershed had estimates of only 16 (meadow 520M15 in

122

Herpetological Conservation and Biology

TABLE 4. Estimates of numbers of Yosemite Toad (Anaryxus canorus) breeding adult males (M), egg masses, male survival (φ), and counts of females (F) encountered from 2006–2009 in six meadows in two watersheds of the Sierra Nevada, California, USA. Number of individuals (# Indiv) is the number of unique male and female toads found during the four year period. Confidence intervals (CI) are 95%.

520M15 520M16 520M20 37188 37213 37165 Value SE CI Value SE CI Value SE CI Value SE CI Value SE CI Value SE CI . M # Indiv 37 19 4 34 27 9 2006 20.6 1.9 19–29 13.6 4.2 11–32 19.2 1.6 18–27 2007 18.7 4.8 14–37 10.1 2.2 8–20 3.0 0.1 3–4 19.4 0.7 19–23 14.3 1.4 13–20 6.2 0.5 6–9 2008 20.1 2.5 17–29 12.0 1.4 11–18 4.0 0.2 4–5 18.2 1.0 18–21 14.2 1.3 13–20 7.2 0.6 7–11 2009 15.9 1.9 14–24 9.1 1.6 8–17 2.0 0.1 2–3 18.3 0.6 18–20 12.0 1.2 11–17 3.1 0.4 3–6

φ 06–07 0.64 0.12 0.39–0.83 0.69 0.12 0.44–0.87 0.71 0.08 0.53–0.85 07–08 0.62 0.11 0.40–0.80 0.68 0.11 0.44–0.86 0.98 0.08 0.01–0.99 0.71 0.08 0.53–0.84 0.49 0.16 0.22–0.76 0.59 0.17 0.27–0.85 08–09 0.57 0.13 0.32–0.79 0.67 0.12 0.41–0.86 0.52 0.26 0.12–0.89 0.72 0.08 0.53–0.85 0.49 0.16 0.22–0.77 0.52 0.17 0.22–0.80

F # Indiv. 18 15 8 38 19 5 2006 11 13 9 2 2007 4 1 6 23 11 3 2008 14 11 2 24 11 5 2009 3 6 2 26 11 0

Eggs 20061 18 0.3 18–20 27 0.5 27–30 17 0.3 15–18 10 0.0 10–10 20072 7 0.2 7–9 19 0.4 19–22 7 0.2 7–9 12 1.0 11–17 7 0.0 7–7 5 0.0 5–5 20082 48 7.6 40–73 28 3.1 25–39 13 0.0 13–13 20 1.3 19–26 16 0.7 16–20 5 0.0 5–5 20093 3 3 1 30 13 4

1Dependent Double Observer Method, 2Independent Double Observer Method, 3Number of egg masses found during surveys. Counts from this method were less influenced by difficulties distinguishing individual masses from communal masses or broken fragments.

2009) to 21 (meadow 520M15 in 2006) and 18 (meadow numbers of egg masses were low, and within the range 37188 in 2008) to 19 (meadow 37188 in 2007) males of the numbers of toads estimated by CMR (Table 4). In each year. One meadow in each watershed had very a few meadow-years, estimates were greater and had small numbers (2–4 and 3–7 males, respectively) each wide confidence intervals. These were in meadows and year. The numbers of males per year was fairly years where distinguishing individual masses from consistent among years, though confidence intervals communal masses or broken fragments was particularly varied. Annual survival estimates for breeding males difficult. In general, the proportion of breeding areas were fairly similar among meadows and among years, with successful metamorphosis was fairly low ranging ranging from a low of 0.49 in meadow 37213 to a high from 0.14 at Bull Creek in 2009 to 0.73 at Highland of 0.71–0.72 in meadow 37188. Only a few toads were Lakes in a wet year (2006, Table 5). Although direct found in meadow 520M20 where survival was 0.98 comparisons are possible for only one year, Highland from 2007–2008. Precision for the survival estimates Lakes generally had more breeding areas with successful was low, likely due to the small sample sizes. Of 130 metamorphosis than Bull Creek based both on unique males captured in the two watersheds, 65 occupancy and our general observations of numbers of (50.0%) were captured in only one year, 34 (26.2%) metamorphs. were captured in two years, 18 (13.8%) were captured in three years, and 13 (10%) were captured in all four Spatial and temporal occupancy patterns.—At the years. Only six males (4.6%) were captured in extensive scale, 93% of the 14 watersheds surveyed nonconsecutive years. annually where breeding was documented were occupied For both the dependent and independent double most years (Fig. 2). A single dry year, 2007, accounted observer approaches used to survey for egg masses, the for most of the documented missed breeding (four of six constant model, p(.), was the best model for each watersheds). The one watershed missing two years was intensive meadow each year and the detection unoccupied in 2007 and 2008. In contrast, evidence of probabilities were high (usually > 0.96). In general, the reproduction was found most years in only 30% of

TABLE 5. Proportion of breeding areas with eggs or tadpoles that had metamorphs for the Yosemite Toad (Anaryxus canorus) from 2006–2009 in two watersheds in the Sierra Nevada, California.

# Breeding Areas With # Breeding Areas With Proportion of Breeding Eggs or Tadpoles Metamorphs Areas with Metamorphs Watershed 2006 2007 2008 2009 2006 2007 2008 2009 2006 2007 2008 2009 Highland Lakes 11 7 11 9 8 3 7 * 0.73 0.43 0.641 * Bull Creek 13 9 12 7 6 * * 1 0.46 * * 0.14 * No surveys were conducted to look for metamorphs. 1Only 2 visits were made at Highland Lakes during 2008, so proportions may have been higher. 123

Brown et al.—Current Status of the Yosemite Toad.

FIGURE 2. Spatial and temporal breeding occupancy patterns for the Yosemite Toad (Anaryxus canorus) in the annual watersheds and intensive meadows including (a) percentage of watersheds, percentage of lakes, meadows, and stream reaches (sites), and percentage of intensive meadow breeding areas that were consistently occupied (occupied all years, unoccupied 1 year) and (b) percentage of annual survey watersheds that had 0, 1–2, or 3+ sites consistently occupied and the percentage of intensive meadows that had 0, 1–2, or 3+ breeding areas consistently occupied.

occupied sites and 49% of breeding areas (intensive conducted for comparison with these monitoring results. meadows). The consistency in occupancy at the During a 1992 resurvey of sites surveyed by Grinnell watershed scale supports our assumption of population and Storer (1924), Drost and Fellers (1996) found the closure for the occupancy estimates. Spatially, more Yosemite Toad had disappeared or declined from 69% than half of the watersheds (64%) had only one or two of the sites (n = 13) and that toad abundances were sites that were consistently occupied with other sites generally low. Jennings and Hayes (1994) found the occupied only in some years (Fig. 2). Fourteen percent species absent in approximately 50% (n = 29) of 55 of the watersheds had three or more sites that were historically occupied localities. No data external to the consistently occupied. Of the intensive meadows, 63% monitoring program exists to evaluate our population had only one or two breeding areas consistently closure assumption for the Yosemite Toad. However, occupied and 38% had three or more breeding areas examination of occupancy in the annual watersheds consistently occupied. In the intensive watersheds, only indicates there has been no obvious violation within this three males moved among meadows during the breeding first monitoring cycle. No trend was apparent and the period though they did move among breeding areas pattern of detection at the watershed scale appeared to be within the meadows. most related to the influences of available water and survey date (Table 1, also see spatial and temporal DISCUSSION occupancy results). Nonetheless, it is possible that our occupancy estimates are high. Based on results from this multi-scale monitoring Yosemite Toad abundance estimates in the two program, we conclude that the Yosemite Toad is still intensive watersheds were much smaller than reported fairly well-distributed but that abundances are low. historical abundances at other locations. During a long- Yosemite Toad occupancy has declined from levels term study at Tioga Pass Meadow, California (1971– observed historically, but toads are still fairly 1982), approximately 2,270 Yosemite Toads were widespread relative to post-1990 records. Only a few marked with annual counts ranging from 162 to 342 assessments of Yosemite Toad occupancy have been males (1974–1979). In six other locations near Tioga

124

Herpetological Conservation and Biology

Pass, three Yosemite Toad populations were reported survival rates for A. boreas of 78% prior to a substantially larger and three had numbers similar to large Bd related population decline (also see Scherer et those found in our intensive meadows (Kagarise al. 2005) and Scherer et al. (2008) reported survival rates Sherman and Morton 1993). Abundances in our ranging from 46% to 86% in uninfected ponds. intensive meadows may have been substantially greater Successful metamorphosis of Yosemite Toads in our in the past. According to Martin (2008), Highland Lakes intensive meadows was generally low, particularly given supported one of the largest breeding populations in the that it was measured by presence rather than number of northern Sierra Nevada. Historical population sizes are metamorphs. Reasons for the low success and apparent unknown, but by the early 1980’s, populations had differences between the Bull Creek and Highland Lakes declined to approximately 50–100 toads in one meadow watersheds are unknown. We are in the preliminary in the watershed (Martin 2008). This is similar to our stages of investigating these results, and at Bull Creek, estimate of abundance in the entire watershed (three our observations suggest that much of the mortality is at meadows) in a given year, suggesting that abundance has the egg and early tadpole development stages. This declined further since that time. The only other analysis would be strengthened by estimating information on historical abundances is qualitative; abundances of metamorphs rather than just presence, historical accounts used terms such as "many males though this is very difficult to do. present", "common" (Grinnell and Storer 1924), and Variable and episodic reproductive success is common "numerous" (Mullally 1953). in aquatic amphibians suggesting that low recruitment in If the abundances found in our intensive watersheds a given year may not necessarily reflect population are reflective of a broader pattern, it may be that declines, particularly for long-lived species like the populations are small rangewide, even though Yosemite Yosemite Toad (Berven 1990; Semlitsch et al. 1996; Toads were found to still occur in many of the Recent Taylor et al. 2006). Yosemite Toad eggs and tadpoles watersheds. Only 18 ± 6.1% of the occupied watersheds are susceptible to a variety of natural stochastic we surveyed rangewide had > 1,000 tadpoles or > 100 environmental events such as freezing and desiccation metamorphs, subadults, or adults detected at the time of resulting in naturally high mortality and low to no survey (Cathy Brown, unpubl. data). Although not all recruitment in some years (Kagarise Sherman 1980; surveys were conducted at the peak of tadpole presence Kagarise Sherman and Morton 1993; pers. obs.). The and adults are not commonly detected outside the persistence of the species over the long-term may breeding period, these data in combination with depend on both high survival rates for the long-lived documented local population declines (e.g., Kagarise adults (15 or more years, Kagarise Sherman and Morton Sherman and Morton 1993; Drost and Fellers 1996) lend 1984) and periodic high recruitment (e.g., Alford and support to the hypothesis that reduced abundances may Richards 1999). This dynamic was explored by Biek et be widespread in Yosemite Toad populations. al. (2002) who found that losses of post-metamorphic Abundances of the closely related Anaxyrus boreas in life stages were more likely to lead to population northeastern Oregon and the Rocky Mountains of declines than losses in the egg or tadpole stages. The Colorado were comparable to the Yosemite Toad importance of both recruitment and adult survival is historical abundances from the Tioga Pass Meadow demonstrated by results from long-term monitoring of an population (Muths et al. 2003; Bull and Carey 2008; A. boreas population in Colorado with abundances Scherer et al. 2008). However, as a result of infection by similar to our larger Yosemite Toad populations. the amphibian chytrid fungus, Batrachochytrium Persistence of the population was sustained by high rates dendrobatidis (Bd), some populations in Colorado have of survival (92% for males) of long-lived adults, but declined to very small numbers (Muths et al. 2003; recruitment was very low (2–5%), and the resulting Muths et al. 2008). Whether Bd is a factor in Yosemite population growth rates showed the population to be in a Toad declines is currently under study (Celeste Dodge, slow decline (Muths and Scherer 2011). pers. comm.). Bd has been found in Yosemite Toads (Green and Kagarise Sherman 2001; Fellers et al. 2011) Temporal and spatial occupancy.—In the majority of and the prevalence varies among populations and both our annual occupied 2–4 km2 watersheds, the Yosemite prevalence and infection intensity is higher on juveniles Toad consistently bred in one or two lakes, meadows, or than on adults (Celeste Dodge, Vance Vredenburg, stream reaches, and then only occasionally in other sites. Cathy Brown, and Amy Lind, unpubl. data). Similarly, in 63% of the intensive meadows, Yosemite No prior estimates of survival and successful Toads consistently bred in one or two of the breeding metamorphosis exist for the Yosemite Toad. The areas, but only occasionally in other locations (Fig. 2b). apparent survival of reproductive males in our intensive Possible explanations include (1) population sizes are meadows was similar or slightly lower than the ranges of too low for toads to breed every year or to saturate the those reported for stable populations of adult male A. available habitat; (2) toads consistently breed in the best boreas in Colorado. For example, Muths et al. (2003) habitat, but occasionally breed in less optimal habitat; or

125

Brown et al.—Current Status of the Yosemite Toad.

(3) some sites have suitable habitat only under certain occupancy data provide affordable robust broad-scale environmental conditions. For example, a site may have information and suggest that the Yosemite Toad is still optimal habitat during high snowpack years but may widespread relative to 1990 distributions, the abundance desiccate prior to metamorphosis during low snowpack data collected in the intensive meadows suggest that years. populations may be small, and the demography data Data from the intensive watersheds provided further provides insights on vital rates. For some species, such insights on how the species uses available habitat spatially as the highly aquatic mountain yellow-legged frogs and temporally. Only a few animals moved among (Rana muscosa and R. sierrae), it may be possible to meadows for breeding, suggesting that Yosemite Toads collect both occupancy and relative abundance data have high site fidelity at the scale of individual bioregionally (Cathy Brown et al., unpubl. data; also meadows. High site fidelity is common to many toad Hecnar and M’Closkey 1997; Bonardi et al. 2011). This species (Breden 1987; Sinsch 1992; Muths et al. 2006). is not feasible given the Yosemite Toad's ecology, and Males did, however, move among breeding areas within even for the mountain yellow-legged frogs, obtaining the meadows. Overall, Yosemite Toads in our study other demographic information (e.g., survival) is not appear to be selecting particular breeding areas, even pragmatic rangewide. though some areas were not used every year. Given the Our monitoring results agree with other studies that fast development of toad eggs and tadpoles, it is likely have found that survey results vary depending on scale. that the breeding areas are chosen based on water Spatially, Hecnar and M'Closkey (1997) concluded that retention and thermal regime. The pattern of snowmelt determination of the status of the Green Frog, Lithobates also may play a role; areas that melt early may be chosen (Rana) clamitans, was dependent on spatial scale and more often for breeding (Olson 1992; pers. obs.). that assessments conducted at smaller scales can lead to Further investigation is needed to better understand these incorrect inferences. We also found that occupancy occupancy patterns including whether the sites and variability depended on scale. Annual variability in breeding areas that are occasionally occupied are a result occupancy at the site scale of individual lakes, meadows, of generally small population sizes or reflect habitat and stream reaches was higher than at the watershed differences and their importance for long-term scale. Given our rotating panel design, single visits at persistence. the site scale once every five years may under represent In our intensive meadows, the proportion of toads occupancy; however, occupancy was fairly consistent found one, two, three, or all four years were similar to from year to year at the watershed scale. Temporally, those reported by Kagarise Sherman (1980) in Tioga longer time series have been shown to be critical for Pass Meadow during a 4-year period (1976–1979). separating short-term fluctuations from longer term Based on capture histories, only 5% of males (n = 6) in trends. Studies have documented large fluctuations in our intensive meadows skipped one or more years. population abundances (Pechmann et al. 1991; Semlitsch Similarly, Kagarise Sherman (1980) found that only 7% et al. 1996; Gibbs et al. 1998; Meyer et al. 1998; Raithel of 522 males captured over multiple years were thought et al. 2011) and site occupancy (Skelly et al. 2003; to have skipped one or more years. Other studies of the Trenham et al. 2003) that occur naturally, but do not closely related A. boreas reported that < 25% (Olson necessarily reflect declines (see Alford and Richards 1992) and 31% (Bull and Carey 2008) of males skipped 1999). We have completed only one monitoring cycle in one or more years of breeding. Muths et al. (2006, the extensive component and the time series for our 2010) found some evidence for temporary emigration in abundance estimates in the intensive meadows is both male and female A. boreas. relatively short (four years). Completion of additional monitoring cycles will determine if our initial spatial and Multi-scale and long term monitoring.—When temporal occupancy and abundance patterns are designing a monitoring program, the information consistent over the long term. objectives and scale are interrelated. There has been a recent emphasis on monitoring occupancy because it is Conservation and management.—Management more feasible for bioregional scale, long-term programs strategies may differ if animals remain in the same sites and it is robust to population fluctuations that have been every year, if different sites are occupied different years documented in many amphibians at local scales (Corn et (e.g., metapopulation, Levins 1970), or if there is a site al. 2005; MacKenzie et al. 2006; Gould et al. 2012). Yet that provides most of the recruitment for a cluster of occupancy is a relatively coarse measure of population sites (mainland, MacArthur and Wilson 1967; source dynamics; declines in abundance may precede the population, Pulliam 1988). For example, if certain sites distributional changes measured by occupancy are always used for breeding then protection could focus (Beiswenger 1986; Collen et al. 2011). Results from this on these. Alternatively, if a variety of sites are used monitoring demonstrate the value of occupancy, from year to year and by different life stages then a abundance, and demography data. The bioregional wider protective zone including connectivity among both

126

Herpetological Conservation and Biology consistently occupied and occasionally occupied sites their help with logistics, administration, and safety. This may be more appropriate. Preliminary interpretation of work was conducted under California Department of our monitoring results in combination with the Fish and Game permit SC-000304. Funding was knowledge that adults use additional habitats (Karlstrom provided by the Pacific Southwest Region, USDA Forest 1962; Kagarise Sherman 1980; Martin 2008; Liang Service. 2010) suggests that a combination of these approaches is warranted. Identification and additional protection for LITERATURE CITED "mainland" breeding sites is clearly important, but our results suggest that management also consider Alford, R.A., and S.J. Richards. 1999. Global incorporating broader protection zones that include adult amphibians declines: a problem in applied ecology. habitats and "island" sites. Further, understanding the Annual Review of Ecology and Systematics 30:133– annual variation of occupancy can inform decisions on 165. monitoring design. For example, if a species is found in Amstrup, S.C., T.L. McDonald, and B.F.J. Manly (Eds.). the same places every year, it may be possible to gain 2005. Handbook of Capture-Recapture Analysis. efficiencies by making less frequent visits to the same Princeton University Press, Princeton, New Jersey, locations. Conversely, if they do not occupy a location USA. every year, it may be necessary to survey more often to Bahls, P. 1992. The status of fish populations and have confidence in trend estimates. Our data suggest management of high mountain lakes in the western that at the watershed scale, occupancy is fairly consistent United States. Northwest Science 66:183–193. from year to year and is strongly related to snowpack. Bailey, L.L., T.R. Simons, and K.H. Pollock. 2004. However, at the site scale, less frequent visits may miss Estimating site occupancy and species detection occupancy in some sites. probability parameters for terrestrial salamanders. The Yosemite Toad appears to have declined over a Ecological Applications 14:692–702. longer time span, yet still persists in the majority of Beebee, T.J.C., and R.A. Griffiths. 2005. The amphibian watersheds occupied since 1990. The declines in decline crisis: a watershed for conservation biology? occupancy from historical locations and the apparent Biological Conservation 125:271–285. small population sizes in at least two locations merit the Beiswenger, R.E. 1986. An endangered species, the development of proactive conservation actions. Wyoming Toad Bufo hemiophrys baxteri – the Research on potential causes and possible mitigation importance of an early warning system. Biological measures is needed. This baseline assessment of status Conservation 37:59–71. provides data to inform management decisions for the Berven, K.A. 1990. Factors affecting population Yosemite Toad and is the foundation for subsequent fluctuations in larval and adult stages of the Wood trend evaluation. By continuing to track trends over Frog (Rana sylvatica). Ecology 71:1599–1608. time, we will be able to evaluate management success Biek, R., C. Funk, B.A. Maxell, and L.S. Mills. 2002. and will provide an early warning system to facilitate What is missing in amphibian decline research: proactive conservation planning. Data collected through insights from ecological sensitivity analysis. the program has given us both quantitative and Conservation Biology 16:728–734. qualitative insights on the status and ecology of this Bonardi, A., R. Manenti, A. Corbetta, V. Ferri, D. sensitive species which benefit its conservation. Fiacchini, G. Giovine, S. Macchi, E. Romanazzi, C. Soccini, L. Bottoni, E. Padoa-Schioppa, and G.F. Acknowledgements.—The design and implementation Ficetola. 2011. Usefulness of volunteer data to of this monitoring program has had input from numerous measure the large scale decline of “common” toad individuals including members of the USDA Forest populations. Biological Conservation 144:2328–2334. Service Sierra Province Assessment and Monitoring Boulanger, J., G.C. White, B.N. McLellan, J. Woods, M. Team. In addition to providing expertise, advice, and Proctor, and S. Himmer. 2002. A meta-analysis of review, Tony Olsen developed the extensive statistical Grizzly Bear DNA mark-recapture projects in British design and analysis and provided the maximum Columbia, Canada. Ursus 13:137–152. likelihood formula, Larissa Bailey provided guidance on Brand, G.J., M.D. Nelson, D.G. Wendt, and K.K. the intensive design and analysis, extensive analysis, and Nimerfro. 2000. The hexagon/panel system for early versions of the manuscript, Amy Lind provided selecting FIA plots under an annual inventory. Pp. 8– review and guidance on the design and final stages of the 13 In Proceedings of the First Annual Forest Inventory manuscript. Amy Lind, Dave Martin, and Walt Sadinski and Analysis Symposium. McRoberts, R.E., G.A. reviewed the original study plan. Jim Baldwin and Tony Reams, and P.C. Van Deusen (Eds.). General Olsen reviewed the statistical text. We thank the hard- Technical Report NC-213 U.S. Department of working field crews of 2002 through 2009, and the Agriculture, Forest Service, North Central Research Stanislaus and other Sierra Nevada National Forests for Station, St. Paul, Minnesota, USA.

127

Brown et al.—Current Status of the Yosemite Toad.

Breden, F. 1987. The effect of post-metamorphic 940. dispersal on the population genetic structure of Gompper, M.E., and H.M. Hackett. 2005. The long- Fowler's Toad, Bufo woodhousei fowleri. Copeia term, range-wide decline of a once common carnivore: 1987:386–395. the Eastern Spotted Skunk (Spilogale putorius). Briggs, J.L., and R.M. Storm. 1970. Growth and Animal Conservation 8:195–201. population structure of the Cascade Frog, Rana Gould W.R.., D.A. Patla, R. Daley, P.S. Corn, B.R. cascadae Slater. Herpetologica 26:283–300. Hossack, R. Bennetts, and C.R. Peterson. 2012. Bull, E.L., and C. Carey. 2008. Breeding frequency of Estimating occupancy in large landscapes: Evaluation Western Toads (Bufo boreas) in northeastern Oregon. of amphibian monitoring in the Greater Yellowstone Herpetological Conservation and Biology 3:282–288. Ecosystem. Wetlands 32:379–389. Burnham, K.P., and D.R. Anderson. 2002. Model Grant, E.H.C, R.E. Jung, J.D. Nichols, and J.E. Hines. Selection and Multimodel Inference: A Practical 2005. Double-observer approach to estimating egg Information-theoretic Approach, 2nd Edition. Springer- mass abundance of pool-breeding amphibians. Verlag, New York, New York, USA. Wetlands Ecology and Management 13:305–320. Cameron, S.A., J.D. Lozier, J.P. Strange, J.B. Koch, N. Green, D.E., and C. Kagarise Sherman. 2001. Diagnostic Cordes, L.F. Solter, and T.L. Griswold. 2011. Patterns histological findings in Yosemite Toads (Bufo of widespread decline in North American bumble canorus) from a die-off in the 1970’s. Journal of bees. Proceedings of the National Academy of Herpetology 35:92–103. Sciences 108:662–667. Grinnell, J., and T.I. Storer. 1924. Animal Life in the Collen, B., L. McRae, S. Deinet, A. De Plama, T. Yosemite. University of California Press, Berkeley, Carranza, N. Cooper, J. Loh, and J.E.M. Baillie. 2011. California, USA. Predicting how populations decline to extinction. Hecnar, S.J., and R.T. M’Closkey. 1997. Spatial scale Philosophical Transactions of the Royal Society B and determination of species status of the Green Frog. 366:2577–2586. Conservation Biology 11:670–682. Corn, P.S., M.J. Adams, W.A. Battaglin, A.L. Gallant, Howat, I.M., and S. Tulaczyk. 2005. Trends in spring D.L. James, M.L. Knutson, C.A. Langtimm, and J.R. snowpack over a half-century of climate warming in Sauer. 2005. Amphibian Research and Monitoring California, USA. Annals of Glaciology 40:151–156. Initiative: Concepts and Implementation. U.S. Jennings, M.R., and M.P. Hayes. 1994. Amphibian and Geological Survey Scientific Investigations Report Reptile Species of Special Concern. Report to the 2005–5015. California Department of Fish and Game. California Corn, P.S., M.L. Jennings, and E. Muths. 1997. Survey Department of Fish and Game, Rancho Cordova, and assessment of amphibian populations in Rocky California. 255 p. Mountain National Park. Northwestern Naturalist Kagarise Sherman, C. 1980. A comparison of the natural 78:34–55. history and mating system of two anurans: Yosemite Crump, M.L., and N.J. Scott. 1994. Visual encounter Toads (Bufo canorus) and Black Toads (Bufo exsul). surveys. Pp. 84–92 In Measuring and Monitoring Ph.D. Dissertation, University of Michigan, Ann Biological Diversity: Standard Methods for Arbor, Michigan, USA. 394 p. Amphibians. Heyer W.R., M.A. Donnelly, R.W. Kagarise Sherman, C., and M.L. Morton. 1984. The toad McDiarmid, L.C. Hayek, and M.S. Foster. (Eds.). that stays on its toes. Natural History 93:72–78. Smithsonian Institution Press, Washington, D.C., USA. Kagarise Sherman, C., and M.L. Morton. 1993. Diaz-Ramos, S., D.L. Stevens, Jr., and A.R. Olsen. 1996. Population declines of Yosemite Toads in the eastern EMAP Statistical Methods Manual. Rep. EPA/620/R- Sierra Nevada of California. Journal of Herpetology 96/002. U.S. Environmental Protection Agency, Office 27:186–198. of Research and Development, NHEERL-WED, Karlstrom, E.L. 1962. The toad genus Bufo in the Sierra Corvallis, Oregon, USA. Nevada of California: ecological and systematic Drost, C.A., and G.M. Fellers. 1996. Collapse of a relationships. University of California Publications in regional frog fauna in the Yosemite area of the Zoology 62:1–104. California Sierra Nevada, USA. Conservation Biology Kendall, W.L. 1999. Robustness of closed capture- 10:414–425. recapture methods to violations of the closure Fellers, G.M., R.A. Cole, D.M. Reinitz, and P.M. assumption. Ecology 80:2517–2525. Kleeman. 2011. Amphibian chytrid fungus Kendall, W.L., and J.E. Hines. 1999. Program (Batrachochytrium dendrobatidis) in coastal and RDSURVIV: An estimation tool for capture-recapture montane California, USA anurans. Herpetological data collected under Pollock's robust design. Bird Conservation and Biology 6:383–394. Study 46 (suppl.):S32–38. Gibbs, J.P., S. Droege, and P. Eagle. 1998. Monitoring Kendall, W.L., J.D. Nichols, and J.E. Hines. 1997. populations of plants and animals. BioScience 48:935– Estimating temporary emigration using capture-

128

Herpetological Conservation and Biology

recapture data with Pollock's Robust Design. Ecology toad, Bufo canorus. Copeia 1953:182–183. 78:563–578. Muths, E., P.S. Corn, A.P. Pessier, and D.E. Green. Knapp, R.A. 1996. Non-native trout in natural lakes of 2003. Evidence for disease-related amphibian decline the Sierra Nevada: an analysis of their distribution and in Colorado. Biological Conservation 110:357–365. impacts on native aquatic biota. Pp. 363–407 In Sierra Muths, E., D.S. Pilliod, and L.L. Livo. 2008. Nevada Ecosystem Project: Final Report to Congress. Distribution and environmental limitations of an Status of the Sierra Nevada. Volume III. Centers for amphibian pathogen in the Rocky Mountains, USA. Water and Wildland Resources, University of Biological Conservation 141:1484–1492. California, Davis, California, USA. Muths, E., R.D. Scherer, P.S. Corn, and B.A. Lambert. Lacan, I., K. Matthews, and K. Feldman. 2008. 2006. Estimation of temporary emigration in male Interaction of an introduced predator with future toads. Ecology 87:1048–1056. effects of climate change in the recruitment dynamics Muths, E., R.D. Scherer, and B.A. Lambert. 2010. of the imperiled Sierra Nevada Yellow-legged Frog Unbiased survival estimates and evidence for skipped (Rana sierrae). Herpetological Conservation and breeding opportunities in females. Methods in Ecology Biology 3:211–223. and Evolution 1:123–130. Levins, R. 1970. Extinction. Pp. 77–107 In Some Muths, E., and R.D. Scherer. 2011. Portrait of a small Mathematical Problems in Biology. Gesternhaber, M. population of Boreal Toads (Anaxyrus boreas). (Ed.). American Mathematical Society, Providence, Herpetologica 67:369–377. Rhode Island, USA. Nichols, J.D., J.E. Hines, J.R. Sauer, F.W. Fallon, J.E. Liang, C.T. 2010. Habitat modeling and movements of Fallon, and P.J. Heglund. 2000. A double-observer the Yosemite Toad (Anaxyrus (= Bufo) canorus) in the approach for estimating detection probability and Sierra Nevada, California. Ph.D. Dissertation, abundance from point counts. Auk 117:393–408. University of California. Davis, California, USA. 126 p. Olsen, A.R., J. Sedransk, D. Edwards, C.A. Gotway, W. MacArthur, R.H., and E.O. Wilson. 1967. The Theory of Liggett, S. Rathbun, K.H. Reckhow, and L.J. Young. Island Biogeography. Princeton University Press, 1999. Statistical issues for monitoring ecological and Princeton, New Jersey, USA. natural resources in the United States. Environmental MacKenzie, D.I., J.D. Nichols, G.B. Lachman, S. Monitoring and Assessment 54:1–45. Droege, J.A. Royle, and C.A. Langtimm. 2002. Olson, D.H. 1992. Ecological susceptibility of Estimating site occupancy rates when detection amphibians to population declines. Pp. 55–62 In probabilities are less than one. Ecology 83:2248–2255. Proceedings of Symposium on Biodiversity of MacKenzie, D.I., J.D. Nichols, J.E. Hines, M.G. Northwestern California. Kerner, H.M. (Ed.). Knutson, and A.D. Franklin. 2003. Estimating site University of California Wildland Resources Center occupancy, colonization and local extinction when a Report 29, Berkeley, California, USA. species is detected imperfectly. Ecology 84:2200– Olson, D.H., W.P. Leonard, and R.B. Bury (Eds.). 1997. 2207. Sampling Amphibians in Lentic Habitats. Northwest MacKenzie, D.I, J.D. Nichols, J.A. Royle, K.H. Pollock, Fauna 4. Society for Northwestern Vertebrate Biology, L.L. Bailey, and J.E. Hines. 2006. Occupancy Olympia, Washington, USA. Estimation and Modeling: Inferring Patterns and Pechmann, J.H.K., D.E. Scott, R.D. Semlitsch, J.P. Dynamics of Species Occurrence. Elsevier, San Diego, Caldwell, L.J. Vitt, and J.W. Gibbons. 1991. Declining California, USA. amphibian populations: the problem of separating Martin, D.L. 2008. Decline, movement and habitat human impacts from natural fluctuations. Science utilization of the Yosemite Toad (Bufo canorus): An 253:892–895. endangered anuran endemic to the Sierra Nevada of Pollock, K.H. 1982. A capture-recapture design robust to California. Ph.D. Dissertation, University of unequal probability of capture. Journal of Wildlife California, Santa Barbara, California, USA. 393 p. Management 46:752–757. Menke, J.W., C. Davis, and P. Beesley. 1996. Rangeland Pradel, R. 1996. Utilization of capture-mark-recapture assessment. Pp. 901–972 In Sierra Nevada Ecosystem for the study of recruitment and population growth Project: Final Report to Congress. Status of the Sierra rate. Biometrics 52:703–709. Nevada. Volume III. Centers for Water and Wildland Pulliam, H.R. 1988. Sources, sinks, and population Resources, University of California, Davis, California, regulation. American Naturalist 132:652–661. USA. Raithel, C. J., P.W.C. Paton, P.S. Pooler, and F.C. Golet. Meyer, A.H., B.R. Schmidt, and K. Grossenbacher. 2011. Assessing long-term population trends of Wood 1998. Analysis of three amphibian populations with Frogs using egg-mass counts. Journal of Herpetology quarter-century long time-series. Proceedings of the 45:23–27. Royal Society of London Series B 265:523–528. Richter, S.C., and R.A. Seigel. 2002. Annual variation in Mullally, D.P. 1953. Observations on the ecology of the the population ecology of the endangered Gopher

129

Brown et al.—Current Status of the Yosemite Toad.

Frog, Rana sevosa Goin and Netting. Copeia and L.A. Jagger. 2003. Regional dynamics of wetland- 2002:962–972. breeding frogs and toads: turnover and synchrony. Scherer, R.D., E. Muths, and B.A. Lambert. 2008. Ecological Applications 13:1522–1532. Effects of weather on survival in populations of Boreal Urquhart, N.S, and T.M. Kincaid. 1999. Designs for Toads in Colorado. Journal of Herpetology 42:508– detecting trend from repeated surveys of ecological 517. resources. Journal of Agricultural, Biological, and Scherer, R.D., E. Muths, B.R. Noon, and P.S. Corn. Environmental Statistics 4:404–414. 2005. An evaluation of weather and disease as causes Urquhart, N.S, S.G. Paulsen, and D.P. Larsen. 1998. of decline in two populations of Boreal Toads. Monitoring for policy-relevant regional trends over Ecological Applications 15:2150–2160. time. Ecological Applications 8:246–257. Schmidt, B. R. 2005. Monitoring the distribution of U.S. Department of Agriculture. 1997. Mapping and pond-breeding amphibians when species are detected digitizing watershed and subwatershed hydrologic unit imperfectly. Aquatic Conservation: Marine and boundaries. National Instruction No. 170–304, USDA Freshwater Ecosystems 15:681–692. Natural Resources Conservation National Cartography Semlitsch, R.D., D.E. Scott, J.H.K. Pechmann, and J.W. and Geospatial Center, Fort Worth, Texas, USA. Gibbons. 1996. Structure and dynamics of an USDA Forest Service. 2001. Sierra Nevada Forest Plan amphibian community: evidence from a 16-year study Amendment (SNFPA) Final Environmental Impact of a natural pond. Pp. 217–248 In Long-term Studies Statement (FEIS). USDA Forest Service, Pacific of Vertebrate Communities. Cody, M.L., and J.A. Southwest Region, San Francisco, California, USA. Smallwood (Eds.). Academic Press, San Diego, U.S. Fish and Wildlife Service. 2002. Endangered and California, USA. threatened wildlife and plants: 12-month finding for a Skelly, D.K., K.L. Yurewicz, E.E. Werner, and R.A. petition to list the Yosemite Toad. Federal Register Relyea. 2003. Estimating decline and distributional 67(237):75834–75843. change in amphibians. Conservation Biology 17:744– Wake, D.B., and V.T. Vredenburg. 2008. Are we in the 751. midst of the sixth mass extinction? A view from the Sinsch, U. 1992. Structure and dynamic of a Natterjack world of amphibians. Proceedings of the National Toad metapopulation (Bufo calamita). Oecologia Academy of Sciences 105:11466–11473. 90:489–499. Weir, L.A., J.A. Royle, P. Nanjappa, and R.E. Jung. Stevens, D.L., Jr., and A.R. Olsen. 1999. Spatially 2005. Modeling anuran detection and site occupancy restricted surveys over time for aquatic resources. on North American Amphibian Monitoring Program Journal of Agricultural, Biological, and Environmental (NAAMP) routes in Maryland. Journal of Herpetology Statistics 4:415–428. 39:627–639. Stevens, D.L., Jr., and A.R. Olsen. 2004. Spatially- Weir, L., I.J. Fiske, and J.A. Royle. 2009. Trends in balanced sampling of natural resources. Journal of the anuran occupancy from northeastern states of the American Statistical Association 99:262–278. North American Amphibian Monitoring Program. Stuart, S.N., J.S. Chanson, N.A. Cox, B.E. Young, Herpetological Conservation and Biology 4:389–402. A.S.L. Rodrigues, D.L. Fischman, and R.W. Waller. White, G.C., D.R. Anderson, K.P. Burnham, and D.L. 2004. Status and trends of amphibian declines and Otis. 1982. Capture-recapture and Removal Methods extinctions worldwide. Science 306:1783–1786. for Sampling Closed Populations. Technical Report Taylor, B.E., D.E. Scott, and J.W. Gibbons. 2006. LA-8787-NERP. Los Alamos National Laboratory, Catastrophic reproductive failure, terrestrial survival, Los Alamos, New Mexico, USA. and persistence of the Marbled Salamander. Williams, B.K., J.D. Nichols, and M.J. Conroy. 2002. Conservation Biology 20:792–801. Analysis and Management of Animal Populations. Trenham, P.C., W.D. Koenig, M.J. Mossman, S.L. Stark, Academic Press, San Diego, California, USA.

130

Herpetological Conservation and Biology

CATHY BROWN, a Wildlife Biologist on the KATIE KIEHL is an Ecologist with the LUCAS WILKINSON is an Ecologist with the Stanislaus National Forest, Sonora, USDA Forest Service on the Stanislaus USDA Forest Service on the Stanislaus California, is the team leader of the USDA National Forest in Sonora, California. After National Forest in Sonora, California. Lucas Forest Service Sierra Nevada Amphibian receiving a B.S. in environmental received a B.A. in Environmental Sciences Monitoring Program. Cathy received her B.S. biology/zoology from Michigan State from Northwestern University and an M.S. in in Conservation and Resource Studies from University, Katie earned an M.S. in biology ecology from the University of Georgia. His the University of California, Berkeley and her from the University of Illinois. She current work focuses on amphibian M.S. in Forest Science from Oregon State currently works on the monitoring and conservation and population ecology in the University, Corvallis, where she studied large conservation of amphibians in the Sierra Sierra Nevada, California. (Photographed by scale population dynamics in pond-breeding Nevada, California. (Photographed by Katie Kiehl) amphibians. She currently works on multi- Celeste Dodge) scale monitoring and conservation of amphibians in the Sierra Nevada, California. (Photographed by Katie Kiehl)

131